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Predictors of hepatitis B and C virus reactivation in patients with psoriasis treated with biologic agents: a 9-year multicenter cohort study

Published:December 07, 2019DOI:https://doi.org/10.1016/j.jaad.2019.12.001

      Background

      The increasing use of biologics is accompanied by a risk of hepatitis B (HBV) and C virus (HCV) reactivation.

      Objective

      To determine the predictors of HBV and HCV reactivation in patients with psoriasis receiving biologics.

      Methods

      This study screened 2060 patients with psoriasis (3562 treatment episodes) who were taking biologics from 2009 to 2018. There were 359 patients with psoriasis with HBV (561 treatment episodes) and 61 with HCV infection (112 treatment episodes).

      Results

      During 8809 and 1522 person-months of follow-up, 88 treatment episodes for HBV involved HBV reactivation, and 14 episodes of HCV involved reactivation. The reactivation rate was significantly higher in treatment episodes of chronic HBV infection than in that of occult HBV (34.3% vs 3.2%, P = .001) and resolved HBV (34.3% vs 5.0%, P < .001). The multivariate analysis revealed that being hepatitis B surface antigen seropositive, being hepatitis B e-antigen seropositive, and tumor necrosis factor-α–inhibitor therapy were risk factors for HBV reactivation, whereas antiviral prophylaxis was effective in reducing the risk of HBV reactivation. No predictors were significantly associated with HCV reactivation.

      Limitations

      Observational design and a lack of a comparison group.

      Conclusion

      Patients with psoriasis on biologics have a risk of HBV and HCV reactivations, particularly those who are seropositive for hepatitis B surface antigen and hepatitis B e-antigen and undergoing tumor necrosis factor-α–inhibitor therapy.

      Key words

      Abbreviations used:

      ALT (alanine transaminase), CHBV (chronic HBV infection), HBcAb (hepatitis B core antibody), HBeAg (hepatitis B e-antigen), HBsAb (hepatitis B surface antibody), HBsAg (hepatitis B surface antigen), HBV (hepatitis B virus), HBVr (HBV reactivation), HCV (hepatitis C virus), HCVr (HCV reactivation), IL (interleukin), IL-12/23i (interleukin-12/23 inhibitor), IL-17i (interleukin-17 inhibitor), RA (rheumatoid arthritis), TE (treatment episode), TNF-α (tumor necrosis factor-α), TNFi (tumor necrosis factor-α inhibitor)
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      References

        • Lavanchy D.
        Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures.
        J Viral Hepat. 2004; 11: 97-107
        • Lavanchy D.
        Evolving epidemiology of hepatitis C virus.
        Clin Microbiol Infect. 2011; 17: 107-115
        • Choi J.
        • Lim Y.S.
        Characteristics, prevention, and management of hepatitis B virus (HBV) reactivation in HBV-infected patients who require immunosuppressive therapy.
        J Infect Dis. 2017; 216: S778-S784
        • Lee H.L.
        • Bae S.H.
        • Jang B.
        • et al.
        Reactivation of hepatitis C virus and its clinical outcomes in patients treated with systemic chemotherapy or immunosuppressive therapy.
        Gut Liver. 2017; 11: 870-877
        • Chiu H.-Y.
        • Wang T.-S.
        • Chen P.-H.
        • et al.
        Psoriasis in Taiwan: from epidemiology to new treatments.
        Dermatol Sin. 2018; 36: 115-123
        • Pompili M.
        • Biolato M.
        • Miele L.
        • et al.
        Tumor necrosis factor-alpha inhibitors and chronic hepatitis C: a comprehensive literature review.
        World J Gastroenterol. 2013; 19: 7867-7873
        • Chiu H.Y.
        • Chen C.H.
        • Wu M.S.
        • et al.
        The safety profile of ustekinumab in the treatment of patients with psoriasis and concurrent hepatitis B or C.
        Br J Dermatol. 2013; 169: 1295-1303
        • Chiu H.Y.
        • Hui R.C.
        • Huang Y.H.
        • et al.
        Safety profile of secukinumab in treatment of patients with psoriasis and concurrent hepatitis B or C: a multicentric prospective cohort study.
        Acta Derm Venereol. 2018; 98: 829-834
        • Chen Y.M.
        • Yang S.S.
        • Chen D.Y.
        Risk-stratified management strategies for HBV reactivation in RA patients receiving biological and targeted therapy: a narrative review.
        J Microbiol Immunol Infect. 2019; 52: 1-8
        • Cho Y.T.
        • Chen C.H.
        • Chiu H.Y.
        • et al.
        Use of anti-tumor necrosis factor-alpha therapy in hepatitis B virus carriers with psoriasis or psoriatic arthritis: a case series in Taiwan.
        J Dermatol. 2012; 39: 269-273
        • Snast I.
        • Atzmony L.
        • Braun M.
        • et al.
        Risk for hepatitis B and C virus reactivation in patients with psoriasis on biologic therapies: a retrospective cohort study and systematic review of the literature.
        J Am Acad Dermatol. 2017; 77: 88-97.e5
        • Sanz-Bueno J.
        • Vanaclocha F.
        • Garcia-Doval I.
        • et al.
        Risk of reactivation of hepatitis B virus infection in psoriasis patients treated with biologics: a retrospective analysis of 20 cases from the BIOBADADERM Database.
        Actas Dermosifiliogr. 2015; 106: 477-482
        • Prignano F.
        • Ricceri F.
        • Pescitelli L.
        • et al.
        Tumour necrosis factor-alpha antagonists in patients with concurrent psoriasis and hepatitis B or hepatitis C: a retrospective analysis of 17 patients.
        Br J Dermatol. 2011; 164: 645-647
        • Navarro R.
        • Vilarrasa E.
        • Herranz P.
        • et al.
        Safety and effectiveness of ustekinumab and antitumour necrosis factor therapy in patients with psoriasis and chronic viral hepatitis B or C: a retrospective, multicentre study in a clinical setting.
        Br J Dermatol. 2013; 168: 609-616
        • Zweegers J.
        • Roosenboom B.
        • van de Kerkhof P.C.
        • et al.
        Frequency and predictors of a high clinical response in patients with psoriasis on biological therapy in daily practice: results from the prospective, multicenter BioCAPTURE cohort.
        Br J Dermatol. 2017; 176: 786-793
        • Hsu H.M.
        • Lu C.F.
        • Lee S.C.
        • et al.
        Seroepidemiologic survey for hepatitis B virus infection in Taiwan: the effect of hepatitis B mass immunization.
        J Infect Dis. 1999; 179: 367-370
        • Chang M.H.
        • Chen C.J.
        • Lai M.S.
        • et al.
        Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group.
        N Engl J Med. 1997; 336: 1855-1859
        • Ni Y.H.
        • Huang L.M.
        • Chang M.H.
        • et al.
        Two decades of universal hepatitis B vaccination in Taiwan: impact and implication for future strategies.
        Gastroenterology. 2007; 132: 1287-1293
        • Manalo I.F.
        • Gilbert K.E.
        • Wu J.J.
        Preventing hepatitis B reactivation associated with immunosuppressive drug treatments for psoriasis.
        J Am Acad Dermatol. 2015; 73: 881-882
        • Torres H.A.
        • Hosry J.
        • Mahale P.
        • et al.
        Hepatitis C virus reactivation in patients receiving cancer treatment: a prospective observational study.
        Hepatology. 2018; 67: 36-47
        • Torres H.A.
        • Davila M.
        Reactivation of hepatitis B virus and hepatitis C virus in patients with cancer.
        Nat Rev Clin Oncol. 2012; 9: 156-166
        • McGovern B.H.
        • Birch C.E.
        • Bowen M.J.
        • et al.
        Improving the diagnosis of acute hepatitis C virus infection with expanded viral load criteria.
        Clin Infect Dis. 2009; 49: 1051-1060
        • Hoofnagle J.H.
        Reactivation of hepatitis B.
        Hepatology. 2009; 49: S156-S165
        • Regev A.
        • Seeff L.B.
        • Merz M.
        • et al.
        Causality assessment for suspected DILI during clinical phases of drug development.
        Drug Saf. 2014; 37: S47-S56
        • Di Bisceglie A.M.
        • Lok A.S.
        • Martin P.
        • et al.
        Recent US Food and Drug Administration warnings on hepatitis B reactivation with immune-suppressing and anticancer drugs: just the tip of the iceberg?.
        Hepatology. 2015; 61: 703-711
        • Lin D.Y.
        • Wei L.J.
        The robust inference for the Cox proportional hazards model.
        J Am Stat Assoc. 1989; 84: 1074-1078
        • Chen M.H.
        • Chen M.H.
        • Liu C.Y.
        • et al.
        Hepatitis B virus reactivation in rheumatoid arthritis patients undergoing biologics treatment.
        J Infect Dis. 2017; 215: 566-573
        • Perez-Alvarez R.
        • Diaz-Lagares C.
        • Garcia-Hernandez F.
        • et al.
        Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases.
        Medicine (Baltimore). 2011; 90: 359-371
        • Fukuda W.
        • Hanyu T.
        • Katayama M.
        • et al.
        Incidence of hepatitis B virus reactivation in patients with resolved infection on immunosuppressive therapy for rheumatic disease: a multicentre, prospective, observational study in Japan.
        Ann Rheum Dis. 2017; 76: 1051-1056
        • Lok A.S.
        • Liang R.H.
        • Chiu E.K.
        • et al.
        Reactivation of hepatitis B virus replication in patients receiving cytotoxic therapy. Report of a prospective study.
        Gastroenterology. 1991; 100: 182-188
        • Ikeda M.
        Reactivation of hepatitis B virus in patients receiving chemotherapy.
        Jpn J Clin Oncol. 2013; 43: 8-16
        • Tsukune Y.
        • Sasaki M.
        • Odajima T.
        • et al.
        Incidence and risk factors of hepatitis B virus reactivation in patients with multiple myeloma in an era with novel agents: a nationwide retrospective study in Japan.
        Blood Cancer J. 2017; 7: 631
        • Yeo W.
        • Chan P.K.
        • Zhong S.
        • et al.
        Frequency of hepatitis B virus reactivation in cancer patients undergoing cytotoxic chemotherapy: a prospective study of 626 patients with identification of risk factors.
        J Med Virol. 2000; 62: 299-307
        • Nagamatsu H.
        • Kumashiro R.
        • Itano S.
        • et al.
        Investigation of associating factors in exacerbation of liver damage after chemotherapy in patients with HBV-related HCC.
        Hepatol Res. 2003; 26: 293-301
        • Chen C.Y.
        • Tien F.M.
        • Cheng A.
        • et al.
        Hepatitis B reactivation among 1962 patients with hematological malignancy in Taiwan.
        BMC Gastroenterol. 2018; 18: 6
        • Yeo W.
        • Zee B.
        • Zhong S.
        • et al.
        Comprehensive analysis of risk factors associating with hepatitis B virus (HBV) reactivation in cancer patients undergoing cytotoxic chemotherapy.
        Br J Cancer. 2004; 90: 1306-1311
        • Zhong S.
        • Yeo W.
        • Schroder C.
        • et al.
        High hepatitis B virus (HBV) DNA viral load is an important risk factor for HBV reactivation in breast cancer patients undergoing cytotoxic chemotherapy.
        J Viral Hepat. 2004; 11: 55-59